Chapters 13 - Life Underground
13. Life Underground
While breaking the blocks of fossil-bearing matrix loose with a large pick, I observed a Leptotyphlops dulcis dissecta and a clutch of eggs fall upon the dirt already loosened for loading. I then saw in the undisturbed bank, in a joint crack, a L. d. dissecta lying upon a clutch of eggs. In another joint crack about 4 in. away was a third blind snake upon a clutch of eggs.
Claude W. Hibbard, 1964
A dirt road running through a marsh in northeastern Illinois was lined with household trash dumped by people too lazy to take the unwanted items to a landfill. Couches, large rugs, sheets of plywood, and roofing tiles were apparently not accepted by the weekly garbage pick-up. It was unsightly, but the trash dramatically increased the habitat for local snakes. Seven species of snakes could be found under or in the debris and on a warm spring or early summer day, more than 100 individual snakes could be seen in an hour’s walk. At the dry edge of the marsh, located under several sheets of plywood, was a large harvester ant nest. Turning the boards nearly always revealed Smooth Green Snakes (Liochlorophis vernalis) [Figure 13–1] and Dekay’s Snakes (Storeria dekayi). Over the last 20 years, much of the wetland has been drained. The roadside debris was cleaned up, a housing development was planted next to remaining wetland, and the snakes disappeared.
INSERT FIGURE 13-1.
Figure 13–1. The Smooth Green Snake (Liochlorophis vernalis). A: An adult. B: A neonate just out of the egg. Smooth Green Snakes are often associated with ant nests, and females will deposit their eggs in ant colonies.
George Pisani reported several small snake species using an active ant nest as a hibernaculum similar to my observations. The snakes used the ant’s tunnels to get below the frost line for the winter. But small colubrid and natricid snakes are not the only snakes known to use ant and termite nests for shelter. John Riley and colleagues listed 17 snakes, mostly tropical, ground dwelling, and arboreal species that lay eggs in ant or termite nests. Riley suggested that at least some of the relationships between the snakes and the insects are probably obligate. The advantages to laying eggs in insect nests are considerable. Temperature and humidity are relatively stable, the eggs may be protected from predators by the insects, and snake eggs in leaf cutter ant nests may be cleaned by the ants to prevent fungal growth. The disadvantages may include the difficulties the female snakes encounter depositing eggs and the escape of the hatchlings from the incubator. Small worm snakes and blind snakes have relatively easy access to the insect nests, but Riley’s list includes some medium-sized caenophidians, such as Chironius, Lamprophis, Liophis, Boiga, and Clelia, as well as the Cat-eyed Snake (Leptodiera annulata). Recently, Boris Baer and co-workers reported finding the eggs of the Cat-eyed Snake in the subterranean fungus garden of the leaf-cutting ant Atta colombica in Panama. The eggs, young, and adults were ignored by the ants, and Baer and colleagues suggest they may have an odor that keeps the ants from recognizing them as intruders.
Following the Ants
In the introductory quote, paleontologist Claude Hibbard stumbled upon a nursery used by the New Mexico Worm Snake, Rena [formerly Leptotyphlops] dissectus. The snakes were 18 inches below the surface and 2 feet back from the exposed bank. The joint cracks were small, and Hibbard described the eggs lying in the cracks, noting that they could not have been laid cross wise in the cavity. Also of interest is his observation of old egg shells from previous years. The New Mexico Worm Snakes had been laying their eggs in these crevices for many years, using them for generational communal nesting. Worm snakes are tiny, well adapted for burrowing, and most species are 12 to 20 cm long and have the diameter of a knitting needle. Worm snakes are ancient; the DNA clock places their origin at 151.9 MYA, and they demonstrate parental care.
Three families of burrowing snakes have been shown to be the most basal of the living snakes in both molecular and morphological studies: the worm snakes (Leptotyphlopidae), the blind snakes (Typhlopidae), and the dawn snakes (Anomalepididae). Collectively, these are called Scolecophidia and they are mostly tropical and subtropical in distribution. And most feed on ant or termite eggs, pupae, or larvae.
Scolecophidians may be mistaken for worms. They have a shiny, slender body, are often uniform in diameter, and the head and tail look alike, making them confusing. Cycloid scales cover the body and there is no trace of enlarged ventral scales. The eyes are greatly reduced and found under the ocular scale; some can detect light, and a few may produce an image on a retina containing only rod cells that function best in dim light. They are incapable of opening their mouth widely and it is tucked well under the skull, which is highly specialized for burrowing head-first through the soil.
The poorly known dawn snakes are found only in the Neotropics. They are distinct from the other two families because they have retained their upper and lower teeth. A recent study by Lillian Parpinelli and Otavio Marques found the Pale-headed Dawn Snake (Liotyphlops beui) to be common within the city limits of São Paulo. This little snake was found to be active during wet - warm periods, and it is nocturnal.
The blind snakes are found throughout most all of the tropical and subtropical world. One typhlopid species, the Braminy Blind Snake (Ramphotyphlops braminus), is composed only of females and has been dispersed over much of the globe by stowing away in potted plants exported from its native Sri Lanka. Blind snakes undoubtedly spend most of their time underground in deserts, grasslands, beaches, and even rainforests, but they are sometimes active on the surface. In the Philippines, Cumming’s Blind Snake (R. cumingii) is a paradox; it climbs into trees and has been found burrowing through the root tangle of epiphytic ferns. It is an arboreal burrower. While typhlopids as a clade are adapted for feeding on ants and termites, the Bismarck Sharp-nosed Blind Snake (Acutotyphlops subocularis) is an earthworm specialist.
The worm snakes (Leptotyphlopidae) inhabit the Neotropics, Africa, and the Middle East, but are absent from Southeast Asia and Australia. Their name comes from their exceptionally slender bodies, which rarely exceed 35 cm in length. All 108 known species are believed to deposit eggs. Worm snakes use a variety of habitats from below sea level to more than 3,200 m above sea level and, like most other scolecophidians, they feed on different stages of social insects.
Julian Watkins and colleagues discovered the Texas Worm Snake (Rena dulcis) [Figure 13–2] crawling in army ant columns as well as inside the ant colonies. Using captured snakes and ants in a test arena, they studied behavioral responses to cloacal sac chemicals from worm snakes and found that it repelled not only small colubrid snakes (ringnecked snakes, Diadophis and milk snakes, Lampropeltis triangulum) that were potential worm snake predators, but it also repelled two potential competitors, the Ground Snake (Sonora episcopa) and the Flat-headed Snake (Tantilla gracilis). Furethmore, it repelled ants. However the the cloacal sac molecules attracted other worm snakes. Secretions from army ants, particularly skatole (a 3-methyl indole), were found to repel all snakes except the worm snake. The fact that worm snakes may use the ant secretions to repel potential predators was supported by lab work. Individual worm snakes without access to ants and their molecules were eaten by ringnecked snakes in the lab. Watkins and colleagues found worm snakes were attracted to live worker ant secretions and extracts of worker ant heads, but they were neither attracted nor repelled by the skatole. This work suggests worm snakes and ants have been engaged in a long term predator-prey relationship that evolved to protect worm snakes from ants as well as snake predators and competitors. In a follow-up study, Fredrick Gehlbach and colleagues showed worm snakes and the Hispaniola Blind Snake (Typhlops pusillus), as well as some colubrids, would follow ant and termite trails and chemical trails of conspecific snakes.
INSERT FIGURE 13-2.
Figure 13–2. A: The Texas Worm Snake (Rena [formerly Leptotyphlops] dulcis) is covered with smooth, cycloid scales. B: The skull (below) is compact and rigid for digging.
Feeding behavior in worm snakes was examined by Nathan Kley and Elizabeth Brainerd. They inverted a dissecting microscope attached to a high-speed video camera and placed it under a clear plexiglas feeding box to film the feeding behavior of these small snakes. They found that the snakes used a unique method to rapidly capture and transport ants and termites into their mouth. The authors wrote, “…these snakes ingest prey by rotating the anterior, tooth-bearing halves of the lower jaw rami rapidly in and out of the mouth like a pair of swinging doors…” The feeding behavior was described as mandibular raking, and Kley and Brainerd stated that it is not likely to represent the primitive feeding mode in snakes despite the basal position of Scolecophidia. Therefore, it is unlikely that the scolecophidians make a good model for a snake ancestor in spite of their basal position in snake phylogeny studies.
Scolecophidians may provide some clues to the geographic origin of snakes. Despite their poor fossil record, their current distribution suggests they arose in Gondwana. The DNA clock dates suggest that blind snakes and worm snakes shared an ancestor about 151.9 MYA (163–137 MYA). Snakes and anguimorph lizards last shared an ancestor about 166 MYA (194–167 MYA). The implication of these dates is that snakes probably diverged from lizards on the paleocontinent. Gondwana broke into western (South America and Africa) and eastern (India, Madagascar, Australia and Antarctica) continents in the Jurassic and early Cretaceous (160–120 MYA) after snakes had evolved. Solny Adalsteinsson and colleagues hypothesize that the worm snakes arose in western Gondwana, while the blind snakes arose in eastern Gondwana. This may have been followed by later dispersal events of typhlopids to other continents in the late Cretaceous or Cenozoic. Western Gondwana separated into South America and Africa about 105–100 MYA. Adalsteinsson and colleagues suggest that worm snake evolution in the New World started about 69–34 MYA, after the separation, and that their ancestor may have been present when South America and Africa separated; or they may have later dispersed from Africa to South America. The burrowing habits of these tiny snakes would seem to make them unlikely global travlers and much remains to be learned about their biology and relationships.
Few ecological studies have been done on scolecophidians, but Godfrey Akani and colleagues studied the Spotted Blind Snake (Typhlops punctatus punctatus) at Rivers State University of Science and Technology, located on the coastal plain of the Gulf of Guinea. They had plots that were 100 m2 and found 207 specimens over a 3-year period; one plot contained 55 specimens. The snakes were found under logs, metallic panels, plastics, stones, and leaf litter. This species showed a preference for loamy soil with 10–18% organic matter, a slightly acidic pH, and it avoided sandy and clay soils. Ants and termites were eaten and only 10% of the collected specimens had empty stomachs, suggesting they feed frequently. One specimen was found in the digestive system of a toad.
At least one advanced snake, a colubrid, searches leaf cutter ant nests for food, but they don’t eat the ants. The poorly known Mexican Short-tailed Snake (Sympholis lippiens) has been found associated with the Mexican leaf-cutter ant (Atta mexicana) nests, and a road killed specimen was found to contain scarb beetle larvae that are commensals with the ants. Therefore, it seems likely that the snake is foraging in the ants’ refuse pits where the beetles lay their eggs. Additionally, this snake has a thick skin which most likely produces chemical repellants to keep the ants at bay.
Confusing Archaic Burrowers
There are several groups of snakes that have been considered intermediate in structure between the scolecophidians and the macrostomates. The intermediate forms have a relatively small gape, eat elongated prey, and burrow. The group includes the dwarf pipe snakes (Anomochilidae, two species known from seven specimens), the Amazon Pipe Snake (Aniliidae, 1 species), the Asian pipe snakes (Cylindrophiidae, 8 species), and the shieldtailed snakes (Uropeltidae, 45 species). The DNA clock suggests these snakes originated 96–89 MYA, and with the exception of the Amazon Pipe Snake (Anilius scytale), they are all Asian in distribution and apparently descended from an early macrostomatan. Their relationships to each other and to other snakes are not well understood. They were previously discussed in Chapter 3.
The forest-covered hills of India’s Western Ghats and the highlands of Sri Lanka are home to a group of unusual snakes related to the Asian pipe snakes (Cylindrophis), the shield-tailed snakes (Uropeltidae). They range in size from 0.2 to 0.8 m in length and have a tail that ends in a blunt tip covered by spine-ornamented scales. Some have tails that look like they were partially split. Carl Gans studied these snakes and described their bizarre heads this way.
… [They] are tiny and ridiculously pointed; the eyes are diminutive; and the lower jaw is countersunk. The nostrils are placed relatively far back and the rostral plate may bear a protruding keratinized keel.
In fact, if they were named for their face instead of their tails it would be appropriate to call them cone-faces. The scales on the body are keratinous, overlap, are exceptionally smooth, and show the iridescence often seen in burrowing species. Why snakes spending their life underground should be iridescent is undoubtedly related to the need to have a smooth body surface that does not collect particulates. They are black, brown, or olive in color with bright stripes or blotches in vivid colors. When captured, the shield-tails hide their head, extend their body, and do their best to attract attention to their tail in a manner similar to that of the the pipe snakes.
Uropeltids eat earthworms. Whether they simply burrow through the soil and eat the worms they encounter, or actively hunt them using the vomeronasal organ or soil vibrations is unclear. However, observations reported by M. V. Rajendran suggest uropeltids use both their VNS and vibrations to locate prey. In one instance, captive snakes came out of burrows to take earthworms dropped into their cage. Another observation reported a snake emerging from a roadside burrow and crawling on to the road to obtain a road-killed earthworm.
The burrowing mechanism these snakes use is a unique apparatus located in the front 25 to 35% of the body. Bends in the forebody are used to propel the head forward into the soil and, as the burrow is extended, more posterior parts of the snake’s trunk are brought forward, widening the tunnel. The anterior muscles are thicker than the more posterior muscles, and they are exceptionly rich in myoglobin and mitochondria in comparison to the posterior muscles. This unique burrowing musculature provides these snakes with the ability to burrow rapidly. In some cases, the burrows follow the roots of trees and Gans suggested that the uropeltid burrowing system may be specifically adapted for traveling along roots.
The patches of bright colors on uropeltids may be used as warnings (aposematic) or to mimic noxious animals. Gans hypothesized that uropeltid colors may mimic the coloration of local elapid snakes or centipedes, and suggested jungle fowl as possible predators. In an experiment using local chickens, he found the birds will eat small uropeltids. When discovered, the snake hid its head under a coil and immediately began digging. While under attack, they have an opportunity to literally dig themselves out of harm’s way while the bird is distracted by the tail.
Uropeltids like cool temperatures and many live in high elevation forests. Recorded body temperatures were between 18 and 22ºC, a range substantially lower than that of other snakes. All species with known reproductive data are live-bearing and produce small litters of offspring. Live birth may allow the females to regulate embryonic development in a cool environment.
Burrowing and Swimming in Sand
There are several groups of boa-like snakes found in North America, Eurasia, Africa, and Madagascar. Their relationships have been controversial, and their morphology has not been helpful in determining how they were related to each other. Brice Noonan and Paul Chippindale used nuclear and mtDNA to examine the relationship between boid snakes and the groups of questionable affinities. They recovered clades that closely correlate to geography. The small North American boa-like snakes, the rubber boa (Charina) and the rosy boa (Lichanura), are not particularly closely related to the sand boas. And the snake commonly called the Burrowing Python (Calabaria reinhardtii) is neither a python nor a boa. Noonan and Chippindale suggested the African Calabaria, the North American boa-like snakes, and the Eurasian sand boas shared their most recent common ancestor about 81 MYA. Calabaria appears to be the sister to two genera of surface-dwelling, boa-like snakes (Acrantophis and Sanzinia) that inhabit Madagascar.
Little is known about the habits of Calabaria, but Francesco Angelici and colleagues radio tracked five specimens in a forested area of southeastern Nigeria. The snakes spent 80% of their time below ground during both the dry and wet seasons, and most above-ground activity was at night. Calabaria used thick forest as well as clearings and swamp forest. They sheltered frequently in termite mounds and social aggregations occurred only during the dry season.
As their name suggests, sand boas are sand burrowers. Daniel Hembree and Stephen Hasiotis used the Kenyan Sand Boa (Eryx colubrinus) in a series of experiments to model trace fossils laid down in loose sediments. In the process, they found sand boas burrow with their head, pushing sediment to the side and then displacing it with side-to-side body movements. This does not compact the soil above the snake, so, as the snake moves forward the burrow behind the snake collapses. In moist soil, the burrow remains open behind the snake but may later collapse as the soil dries out. The sand boas remained below the surface for several hours and would occasionally move their body to compress the soil and enlarge the cavity they inhabited.
Using the North American Rubber Boa (Charina bottae) as a basal macrostomate, Javier Rodriguez-Rob les and co-workers examined gape size and diet in this ancient snake lineage and compared its diet to that of the sand boas. Small Rubber Boas feed on squamate eggs and lizards, which requires both active foraging and ambush feeding strategies. However, as the snakes grow, they shift to birds and mammals. The researchers found a high percentage of tail-first ingested prey, suggesting that adult Rubber Boas were taking nestling birds and mammals. The sand boas also used both ambush and active foraging, feeding on adult birds and rodents. Current evidence suggests these small, boa-like snakes appeared in the fossil record about the same time (the Paleocene) as rodents, a coincidence that may have stimulated the evolution of a larger gape in the early macrostomates.
Many different lineages of caenophidian snakes contain burrowing species, including the colubroids and elapoids. Reduced eyes, a thin body of a uniform diameter, a short tail, and a low number of dorsal scale rows are characteristics of snakes that are extreme burrowers. The three families of burrowing scolecophidians share these traits, but some colubroid and elapoid snakes have evolved this extreme burrowing morphology.
One colubroid showing some extreme burrowing morphology is Colubroelaps nguyenvansangi. It was described in 2009 by Nicolai Orlov and co-workers. The new genus and species was based upon a single female specimen collected in southern Vietnam, about 720 m above sea level in a forest with exceptionally large trees. The half-meter long snake was found under the leaf litter. It is exceptionally thin (the body's diameter is about 6 to 8 mm) and it has 279 trunk vertebrae and another 83 tail vertebrae. Glance at the photos of this snake and it superficially appears to be a scolecophidian, but close examination shows that it is a colubroid. The length of the tail is a good clue. Scolecophidians usually have fewer than 30 tail vertebrae. Orlov and colleagues tentatively assigned this snake to the family Colubridae, but its true relationships remain to be discovered.
The Western Shovel-nosed Snake (Chionactis occipitalis) is a colubrid that has evolved some extreme morphology and behaviors for sand swimming. It has a countersunk lower jaw, valves in its nostrils, and a spade-shaped head for pushing through sand. Because sand acts more like a fluid than a solid, the term “sand swimming” is quite appropriate. Chionactis is restricted to the deserts of the American southwest and northern Mexico, and it spends the day below ground, emerging at night to hunt scorpions. Kenneth Norris and J. Lee Kavanau observed Chionactis appearing suddenly and in synchrony while the authors were road hunting for snakes. Norris and Kavanau conducted a behavioral study using fossorial chambers equipped to monitor snake activity, oxygen levels, temperature, and pressure. The snakes showed a distinct daily rhythm of activity composed of nocturnal activity on the surface and diurnal resting periods. Interestingly, they found Chionactis did not simply wait below the surface for the temperature to drop. Instead, activity increased 24 hours or less after their last visit to the surface, behavior apparently regulated by the snake’s internal clock. Below the surface the snake changed from using its throat, rather than abdominal, muscles to breathe probably because of the pressure of the sand on its body. When submerging into the sand, the snake arches its forebody so that the snout is below the ventral surface of the body. The space behind the rostral scale is usually clear of sand, and as the snake exhales, sand is blown away from the nostrils. To capture a scorpion, the snake seizes the prey at the base of the stinger and moves the scorpion into its mouth on the side opposite the stinger. In some cases, the snake backs into the sand, bringing the scorpion with it. The arachnid is bent into a U-shape and, when the snake gets to the legs, it swallows the stinger and the legs simultaneously to avoid envenomation.
The Bandy-bandy (Vermicella annulata) is a highly specialized, subterranean Australian elapid that feeds exclusively on blind snakes (Typhlopidae) which may be much longer than they are. Matthew Greenlees and co-workers tested the Bandy-bandy’s ability to follow the chemical trail of the Blackish Blindsnake (Ramphotyphlops nigrescens) and found that it ignored the chemical trails laid down by other squamates and a distilled water control, and followed the odor of the blindsnake. Greenlees and colleagues have observed this snake raising its head off the substrate, waving it from side to side, and flicking their tongue into the air. The authors suggested this behavior is an attempt to pick up odors of more recent trails. Undoubtedly, Vermicella most often finds the blind snakes in sub-surface tunnels and feeds on them underground.
In Western Australia’s Great Victoria Desert there is a community of five fossorial elapids. Stephen Goodyear and Eric Pianka examined the burrowing elapid community in an attempt to understand how they partition resources. The Desert Banded Snake (Simoselaps anomalus) used the crests of ridges, while Jan’s Banded Snake (Simoselaps bertholdi) and the Southern Shovel-nosed Snake (Brachyurophis semifasciatus) were found in all microhabitats in about equal numbers. The Narrow-banded Shovel-nosed Snake (Brachyurophis fasciolatus) and the Black-naped Snake (Neelaps bimaculatus) were trapped about half the time on slopes, but never in flat areas. The Desert-banded Snake and Jan’s Banded Snake fed almost exclusively on slider skinks of the genus Lerista. Only one prey item was identified from the Black-naped Snake, the tail of a blind snake, and the Narrow-banded Shovel-nosed Snake feeds exclusively on squamate eggs. The authors found that all of these snakes are nocturnal, produce small numbers of eggs, and are most active in November and December.
The two species of South African shieldnose snakes (Aspidelaps) are fossorial elapids that feed on frogs, other snakes, and mammals. These unique elapids have stubby bodies compared to most members of their family and Richard Shine and colleagues have suggested this may indicate they are ambush foragers. Male Shieldnose Snakes (A. scutatus) have smaller heads than females and consumed more frogs, suggesting that head size may be correlated to diet, although the study’s sample size was relatively small. Female shieldnose snakes are known to attend to their eggs. Shieldnose snakes have a cobra-like defensive behavior that includes the display of a narrow hood. Molecular studies suggest they are the sister to the Desert Black Snake (Walterinnesia aegyptia) of northeast Africa and the Middle East. Both these genera favor arid environments, are nocturnal, and use burrows.
Vipers ,too, have adapted to life on and below the sand. The Sidewinder (Crotalus cerastes) uses sand dunes and specialized locomotion (sidewinding) for moving across loose sand. Middle Eastern and African sand vipers of the genus Cerastes have the unique ability to burrow vertically into the sand and cover themselves with sand so they are completely out of sight. Bruce Young and Malinda Morain examined this behavior and found the key to the snake’s successful submergence lies in localized unilateral rib abduction. The ribs of these snakes end in expanded, calcified costal cartilages. When the rib is abducted, it moves the sand from under the snake off to the side. The researchers found they could inhibit burrowing behavior by taping portions of snakes’ body to prevent rib abduction. Young and Morain found that the snakes were unable to bury taped segments. This type of burrowing behavior may be used to escape predators, ambush prey, or regulate body temperature, and the authors found Cerastes vipera always struck prey from below the sand. Other vipers highly adapted to life in the sand include Pseudocerastes and Eristicophis.
Hunting in Burrows and Digging Tunnels
The stiletto snakes (Atractaspis) of the African Burrowing Snake family (Atractaspididae) are thought to have originated about 33 MYA. They are most specious in Africa and are nested in a larger radiation of African snakes, the superfamily Elapoidae. Richard Shine and colleagues examined six species of stiletto snakes and found diverse diets. The quill- snouted snakes (Xenoclamaus) feed on amphisbaenians while the stiletto snakes (Atractaspis), purple-glossy snakes (Amblyodipsas), and the Natal black snake (Macrelaps) fed on snakes and burrowing skinks. Mammals composed less than 25% of the prey recovered from 71 specimens. The authors posit that the side-stabbing behavior used for envenomation (discussed in Chapter 5) evolved with the need to envenomate prey in narrow burrows and to overcome the challenges squamate prey present by blocking burrows to impede pursuit by tail autotomy. Atractaspidids have small bodies and often quill-shaped heads (like Xenoclamus); both are useful for following prey into burrows. When the burrow is blocked by the prey’s body, the flat, pointed head can be slid forward between the burrow wall and the prey’s body, a fang can be extended to the side, and the snake can pull its head backwards to envenomate the prey. Shine and colleagues suggest that, via this tactic, tail autotomy in lizards could block a burrow and impede a predator’s movement while the prey escapes without its tail, but avoids envenomation.
Acts of predation by burrowing snakes are difficult to observe because their behavior occurs below ground. Consequently, interested zoologists need to depend on stomach contents for information. David Gower and colleagues reported an adult caecilian taken from the gut of a Slender Burrowing Stiletto Snake (Atractaspis aterrima). The network of tunnels made by a variety of animals can serve as the hunting grounds for these subterranean snakes.
Snakes that make their own burrows and spend most of their lives underground are usually small, but there are exceptions. The North America genus Pituophis contains some of the largest snakes (pine snakes, gopher snakes, and bullsnakes) on the continent, and they are expert burrowers [Figure 13–3]. Pituophis forages in burrows and may co-opt mammal burrows for its own refuge, but it has also been known to dig its own. Charles Carpenter made extensive observations on burrowing behavior in the Bullsnake (Pituophis catenifer sayi) in an environmental chamber equipped with video cameras. The spade-shaped head was used to scoop sand that was then moved posteriorly with a head-forebody flexure. The soil was then moved away from the excavation. Carpenter estimated a Bullsnake could move 3,400 cm3 of soil per hour. Pituophis responded strongly to soil with the scent of Pocket Gophers (Geomys bursarius), and snakes attempted to enlarge Pocket Gopher burrows to reach the rodents.
INSERT FIGURE 13-3.
Figure 13–3. A Bullsnake (Pituophis catenifer sayi) that has been digging.
Given their size, it is somewhat surprising that female Pituophis will dig their own nests. Nest tunnels may run almost 3 m in length. Joanna Burger and Rob ert Zappalorti studied nest site selection by the Pine Snake (P. melanoleucus) in the New Jersey Pine Barrens. They reported on 22 nesting sites, about half of which were communal nests. Females selected sites that maximized exposure to the sun; there was usually less than 5% canopy cover, and ground vegetation was sparse. The sandy soil at nest sites was usually looser than randomly selected sites, and the soil was moist below 15 cm. Unexpectedly, only one of 20 nests was located in an undisturbed location. Females frequently select man-made clearing such as open areas near roads or other disturbed areas. Female pine snakes start testing the soil for suitable locations in mid June by pressing their snout into the soil about 2 cm start, making test holes, beginning an excavation, and then stopping, apparently deciding a location is unsuitable. If a digging snake encounters roots during the excavation, it changes direction. Females excavate in the early morning and again in the late afternoon, and it takes two to four days to complete a nest. Eggs are laid during a two-week period between mid June and mid July. Burger and Zappalorti found 73% of the nests had old eggshells present, suggesting certain sites were favored and perennial. The eggs were deposited in a chamber 21 to 22 cm below ground, and many nests were used by multiple females.
Burrows provide a secure refuge for snakes. They may represent the original microhabitat for the snake ancestor, and they make studying snakes that use them a challenge. Burrowing snakes also offer herpetologists the opportunity to discover new adaptations to underground lifestyles. To be sure, many burrowing snake species have yet to be described, and the known species still have intriguing natural histories waiting to be discovered.
